Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance

J. L. Bi, G. W. Felton

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Abstract

Oxidative responses of plants to pathogens and other environmental stresses have received considerable recent attention. We propose that an oxidative response also occurs following attack by herbivores. Our data strongly indicate a shift in the oxidative status of soybean following herbivory by the insect Helicoverpa zea. Herbivory caused significant increases in lipid peroxidation and ·OH radical formation. The activity of several oxidative enzymes including lipoxygenases, peroxidase, diamine oxidase, ascorbate oxidase, and NADH oxidase I increased after herbivory on soybean. The enhanced production of phenolic compounds is indicated by an increase in the activity of phenylalanine ammonia lyase in wounded tissues. On the other hand, the level of soybean foliar antioxidants such as ascorbic acid, total carotenoids, nonprotein thiols, and catalase decreased significantly following herbivory. These results implicate primary compounds (e.g., ascorbic acid, proteins), secondary metabolites (e.g., phenolics), and reactive oxygen species (e.g., hydroxyl radical, hydrogen peroxide) as multiple components of induced resistance. The oxidative changes in the host plant correspond with increased oxidative damage in the midgut of insects feeding on previously wounded plants. Decreases in nonprotein thiols and reduced ascorbic acid occurred in midgut epithelial tissue from insects feeding on wounded plants compared to the insects on control plants. In contrast, midgut hydroperoxides and dehydroascorbic acid concentrations were greater in insects on wounded plants compared to their counterparts on control plants. We conclude that oxidative responses in soybean may have both positive and negative effects upon the host plant: a decrease in herbivory and an increase in oxidative damage to the plant. The salient benefit to the plant, in terms of insect resistance, is the relative balance between these opposing effects.

Original languageEnglish (US)
Pages (from-to)1511-1530
Number of pages20
JournalJournal of Chemical Ecology
Volume21
Issue number10
DOIs
StatePublished - Oct 1 1995

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All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry

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